Comparative study on synteny between yeasts and vertebrates

C. R. Biologies 334 (2011) 629–638
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Evolution/Évolution
Comparative study on synteny between yeasts and vertebrates
Étude comparative de la synténie chez les levures et chez les vertébrés
Guénola Drillon, Gilles Fischer *
CNRS UMR7238, laboratoire de génomique des microorganismes, université Pierre-et-Marie-Curie, institut des Cordeliers, 15, rue de l’École-de-médecine,
75006 Paris, France
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 7 November 2010
Accepted after revision 29 March 2011
Available online 5 July 2011
We studied synteny conservation between 18 yeast species and 13 vertebrate species in
order to provide a comparative analysis of the chromosomal plasticity in these 2 phyla. By
computing the regions of conserved synteny between all pairwise combinations of species
within each group, we show that in vertebrates, the number of conserved synteny blocks
exponentially increases along with the divergence between orthologous protein and that
concomitantly; the number of genes per block exponentially decreases. The same trends
are found in yeasts but only when the mean protein divergence between orthologs
remains below 36%. When the average protein divergence exceeds this threshold, the total
number of recognizable synteny blocks gradually decreases due to the repeated
accumulation of rearrangements. We also show that rearrangement rates are on average
3-fold higher in vertebrates than in yeasts, and are estimated to be of 2 rearrangements/
Myr. However, the genome sizes being on average 200 times larger in vertebrates than in
yeasts, the normalized rates of chromosome rearrangements (per Mb) are about 50-fold
higher in yeast than in vertebrate genomes.
ß 2011 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved.
Keywords:
Yeast
Vertebrate
Synteny
Genome
Evolution
Chromosome
Rearrangements
R É S U M É
Mots clés :
Levures
Vertébrés
Synténie
Génome
Evolution
Chromosome
Réarrangements
Nous avons étudié la conservation de la synténie entre toutes les combinaisons deux à
deux de 13 génomes de vertébrés et de 18 génomes de levures dans le but de fournir une
analyse comparative de la plasticité chromosomique de ces 2 Phyla. En calculant les
régions de synténie conservée entre toutes les paires d’espèces au sein de chaque groupe,
nous montrons que chez les vertébrés, le nombre de blocs synténie augmente de façon
exponentielle avec la divergence entre protéines orthologues et que de façon
concomitante, le nombre de gènes par bloc décroı̂t de façon exponentielle. Chez les
levures, on observe les mêmes tendances mais lorsque la divergence protéique dépasse
36 %, le nombre de blocs diminue graduellement. Nous montrons également que les taux
de réarrangements sont en moyenne 3 fois plus élevé chez les vertébrés que chez les
levures et correspondent à une valeur de 2 réarrangements/Ma. Cependant, les génomes
étant en moyenne 200 fois plus gros chez les vertébrés que chez les levures ; les taux
normalisés de réarrangements chromosomiques (par Mb) sont environ 50 fois plus élevés
dans les génomes de levures que dans les génomes de vertébrés.
ß 2011 Académie des sciences. Publié par Elsevier Masson SAS. Tous droits réservés.
* Corresponding author.
E-mail address: gilles.fi[email protected] (G. Fischer).
1631-0691/$ – see front matter ß 2011 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.crvi.2011.05.011
630
G. Drillon, G. Fischer / C. R. Biologies 334 (2011) 629–638
1. Synteny, an old genetic concept with a new meaning
in comparative genomics
1.1. Synteny in the ‘‘linkage’’ sense
The first use of the word synteny dates back to the early
seventies (Fig. 1) when new methods for gene mapping
based on somatic hybrid cell lines were developed.
Synteny originally described the colocalization of several
markers on the same chromosome. As human chromosomes were preferentially lost in man-rodent hybrid cells,
two genes could be attributed to the same chromosome
when simultaneously present or absent from a hybrid cell
population whatever the genetic distance separating them.
These physically linked, but not necessarily genetically
linked, genes were called syntenic genes. Etymologically,
the term synteny means ‘‘on the same ribbon’’ (from the
Greek syn = together and taenia = ribbon). Although relatively limited in number until the 1990s, nearly all
published scientific papers referring to synteny involved
gene mapping studies based on hybrid somatic cells in
human and also in many primate, cattle and rodent species
[1–4]. These methods led to the development of highdensity radiation hybrid maps during the 1990s [5]. In the
last 20 years, the number of synteny-related papers
published each year has linearly increased to reach more
than 200 scientific reports in the year 2009. It is interesting
to
[(Fig._1)TD$IG] note that in yeast, the number of publications dealing
with synteny has always been quantitatively negligible
since this term was first invented (Fig. 1). However, several
experimental studies based on electrophoretic karyotyping and later on, on comparative genomic hybridization,
have allowed an exploration of the chromosome structures
and their evolution in yeast [6–11].
1.2. Synteny in the conserved gene order sense
Chromosomes do not remain collinear over evolutionary time because rearrangements such as translocations,
inversions, duplications and deletions shuffle the order
and orientation of large genomic segments between
genomes. When genetic maps became available for several
related species, researchers started to compare genomes in
order to understand how chromosomes are evolving. In
this context, the notion of shared-synteny (or synteny
conservation) was increasingly used in the literature.
However, this notion was employed with a meaning
different from the original definition of synteny. Instead of
describing the linkage of genes on chromosomes in
different species, the concept of shared-synteny rather
described the preservation of gene order between homologs along chromosome segments in different species.
Some geneticists rejected this use of the term synteny and
noticed that a majority of the scientific papers did not use
the term synteny according to its original meaning [12]. It
is probably because a term of reference was lacking to
Fig. 1. The use of the term synteny in the scientific literature. The ‘Synteny’ plot (open squares) corresponds to the total number of publications citing the
word synteny in either the title or the abstract sections identified in PubMed between 1970 and 2009. The ‘synteny in vertebrates’ plot (open triangles)
corresponds to the fraction of these publications that in addition comprises one of the following terms: mammal* or mouse or human or primate or fish or
cattle or rodent or dog or rat or mouse or vertebrate*, in either the title or the abstract sections. The ‘synteny in yeasts’ plot (open circles) corresponds to the
fraction of the total synteny publications that comprises one of the following terms: yeast* or Saccharomyces or Candida or Kluyveromyces, in either the title
or the abstract sections, followed by manual curation to remove publications citing yeast for methodological reasons (such as YAC). The black curve
represents the number of completely sequenced genomes (eukaryotes, bacteria and archaea) published and referenced in the Genome OnLine Database
(http://www.genomesonline.org/). From the year 2000 where the number of completely sequenced genomes rapidly increased, the relative prominence of
vertebrates (open triangles) in the synteny-related literature has partly declined probably to the profit of plant and bacteria studies while the total number
of publications dealing with yeast in the field of synteny (open circles) has always remained anecdotic.
G. Drillon, G. Fischer / C. R. Biologies 334 (2011) 629–638
describe the conserved order of common markers in
different species that the term ‘‘shared synteny’’ has been
diverted from its original meaning. Subsequently, this term
was gradually stripped of the word ‘‘shared’’ (or conserved)
and in today’s researcher’s vocabulary, synteny, on its own,
(abusively) means conserved gene order between different
species rather than linkage of two or more markers on a
chromosome per se.
In the last decade, sequencing technologies have taken
over traditional methods of gene mapping. With the
growing availability of genome sequences, the large
prominence of vertebrates in the synteny-related literature has partly declined (Fig. 1) probably to the profit of
plant and bacteria studies (Fig. 1). Concomitantly, synteny
studies have moved from the experimental field to the
bioinformatics field. Although the total number of publications dealing with yeast in the field of synteny has
remained anecdotic (Fig. 1), pioneering genome-wide
explorations of gene content and gene order based on
sequencing data only were first developed between related
yeast species [13–16]. These studies paved the road for the
birth of a new field called comparative genomics aiming at
understanding the mechanisms of genome evolution
through the comparative analysis of chromosomes between related species. Comparative genomics was concomitantly developed in vertebrates, with the sequencing
of a compact fish genome, Tetraodon nigroviridis [17], to
help for the annotation of the human genome [18,19], as
well as in yeast with the Génolevures program [20] which
631
represented the first large exploratory sequencing project
between related species aiming at deciphering the
mechanisms of genome evolution. Among other things,
the Génolevures 1 program sought for the mechanisms of
chromosome map reorganization through the study of
synteny conservation [21]. Since then, the study of synteny
has been the tool of choice, both in yeasts and vertebrates, to
unravel major conceptual advances in our understanding of
genome evolution such as orthology/paralogy relationships
and the relative contributions of segmental vs whole
genome duplication (WGD) events. Synteny has also
allowed the determination of the relative rates of chromosome rearrangements in individual lineages of yeast and
vertebrate as well as the reconstruction of ancestral
genomes. Finally, the study of the structure and the
repartition of synteny breakpoints gives access the mechanisms of chromosome rearrangements and to the models of
genome evolution. However, no study has so far put into
perspective the relative levels and rates of chromosomal
reorganization between yeast and vertebrates.
2. The evolution of synteny in yeasts and vertebrates
2.1. Major structural and functional differences between
yeast and vertebrate genomes
Yeasts and vertebrates harbor very different genome
characteristics in terms of size (a 200-fold difference on
average, Table 1), number of genes, proportion and size of
Table 1
List of the 18 yeast and 13 vertebrate species with completed genome sequences.
Class
Species
Genome size (Mb)
Chromosome number
Scaffold number
Reference
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Saccharomycetes
Mammalia
Actinopterygii
Mammalia
Aves
Mammalia
Mammalia
Mammalia
Marsupialia
Actinopterygii
Mammalia
Mammalia
Aves
Actinopterygii
Candida albicans
Candida dubliniensis
Candida glabrata
Candida tropicalis
Clavispora lusitaniae
Debaryomyces hansenii
Eremothecium gossypii
Kluyveromyces lactis
Lachancea kluyveri
Lachancea thermotolerans
Lachancea waltii
Lodderomyces elongisporus
Pichia guilliermondii
Pichia pastoris
Pichia stipitis
Saccharomyces cerevisiae
Yarrowia lipolytica
Zygosaccharomyces rouxii
Canis familiaris
Danio rerio
Equus caballus
Gallus gallus
Homo sapiens
Macaca mulatta
Mus musculus
Opos monodelphis
Oryzias latipes
Pan troglodytes
Ratus Norvegicus
Taeniopygia guttata
Tetraodon nigroviridis
14.3
14.6
12.3
14.6
12.1
12.2
8.7
10.7
11.3
10.4
10.7
15.5
10.6
9.4
15.4
12.1
20.5
9.8
2400
1700
2689
1000
3080
2871
2644
3475
800
3100
3000
2644
350
8
8a
13
8
8
7
7
6
8
8
8
9
8
4
8
16
6
7
39
25
32
40b
23
22
20
9
24
24
21
28
21
8
8a
13
23
9
7
7
6
8
8
10
27
9
6
9
16
6
7
39
25
32
30
23
21
20
9
24
22
21
29
21
[44]
[45]
[35]
[46]
[46]
[35]
[47]
[35]
[48]
[48]
[49]
[46]
[46]
[50,51]
[52]
[53]
[35]
[48]
[54]
Unpublished
[55]
[56]
[18,19]
[57]
[58]
[59]
[60]
[61]
[62]
[63]
[36]
a
b
Pseudochromosomes obtained by mapping onto C. albicans chromosomes [45].
Including microchromosomes that were not assembled.
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G. Drillon, G. Fischer / C. R. Biologies 334 (2011) 629–638
introns, number of transposable elements and repeat
sequences, gene density and proportion of coding and
noncoding DNA (see [22] and [23] for a review of yeast and
vertebrate genome architectures, respectively). In addition, major functional properties that can have a profound
impact onto genome dynamics also differ between yeasts
and vertebrates. Firstly, outcrossing between germ lines is
the only mode of propagation of vertebrates, implying that
the chromosome rearrangements that can be transmitted
to the next generation and eventually reach fixation in
populations are restricted to the meiotic divisions and the
subsequent mitotic amplification of the gamete cell lines.
The life cycle of wild yeasts is more complex, including
clonal reproduction, outcrossing, and inbreeding. Yeast
reproduction is principally characterized by a rapid clonal
expansion when the environmental conditions are favorable. The proportion of sexual reproduction varies between
lineages. Many lineages seem to be completely asexual
while for those that undergo meiosis, mating mainly occur
between ascospores originating from the same tetrad
(inbreeding), hence limiting the level of outcrossing. It was
calculated that Saccharomyces species undergo one sexual
cycle every 1000 asexual divisions and that the proportion
of outcrossing would be limited to once in every 50,000 to
100,000 asexual generations [24,25]. The rates of meiotic
recombination are also very different because 1 centimorgan corresponds to approximately 3 kb in yeast but to
about 1 Mb in human [26]. This implies that the two
organisms have similar genome sizes in centimorgans.
Secondly, it is well known that mitotic mutation rates vary
between organisms [27,28]. From recent sequencing data,
the intergeneration substitution rate is estimated to
1.1 10 8 per base per human haploid genome [29] and
about 3 10 10 per base per division in either diploid or
haploid cells of Saccharomyces cerevisiae [30,31]. These
figures correspond to a 36-fold difference in the per-base
probability of mutation. This difference is probably due to
the cell divisions that occur in the germ line between two
generations in human, while in yeast, one cell division
corresponds to one asexual generation. In human, the
number of cell divisions in the germ line per generation is
limited to 30 cell divisions in women because oogonia
cease replication during fetal life but is close to 200
divisions in a 20 year old man where spermatogenesis
takes place throughout life [32]. Finally, another major
functional difference between yeasts and vertebrates is the
generation time that could differ by several orders of
magnitude (few hours in yeasts compared to few months
or years in vertebrates). This implies that for a similar
evolutionary time the number of generations would be
much higher in yeasts than in vertebrates although the
average generation time for yeast populations in natural
environments must be much longer than a few hours
because they would often have to face critical growth
conditions (such as long periods of starvation, low
temperatures, etc.).
2.2. Chromosome evolution in yeasts and vertebrates
Because of these radically different structural and
functional properties and also because important efforts to
understanding genome evolution have been made so far
separately in yeasts and vertebrates, it was interesting to
compare the dynamics of chromosome map reshuffling
between these two groups of eukaryotes. Large sequencing
data sets are presently available for 51 vertebrates (http://
www.ensembl.org/index.html) and 32 yeasts from the
Saccharomycotina subphylum [33]. However, there is a
great diversity in the completeness of genome sequences.
Because fragmented genome assemblies would introduce
a high number of artificial synteny breakpoints, we
excluded species where the genome sequence is broken
into too many small contigs and focused on the 13
vertebrate genomes and the 18 yeast genomes for which
chromosomes are represented by a single or a limited
number of sequencing scaffolds (Table 1).
To look for common or different evolutionary themes
and to test whether there exists some sort of molecular
clock for chromosome rearrangements, we computed the
blocks of conserved synteny between all pairs of species
applying exactly the same criteria (see legend of Fig. 2) to
the 78 and 153 possible pairwise comparisons of species
within the groups of vertebrates and yeasts, respectively. A
unit to measure evolutionary time that would be common
to both yeast and vertebrate is nevertheless needed in
order to compare the evolution of the number and the size
of synteny blocks in these two groups of species.
Estimations of evolutionary time in Myr for yeast are
weak due to the absence of reliable fossil records. In
addition, generation times are very different between
yeasts and vertebrates. Therefore, we decided to use the
average protein divergence between orthologs as the
common unit of evolutionary range. Previous analyses
using the global level of divergence of orthologous proteins
revealed that the evolutionary range covered by the
Saccharomycotina yeasts exceeds that of vertebrates and
is similar to the span covered by the entire phylum of
Chordata [34–36].
In vertebrates, the number of synteny blocks increases
exponentially with increasing divergence time, varying
from a very small number of blocks, 43 between human
and chimpanzee, to more than 1900 blocks between dog
and zebrafish (Fig. 2a). The highest numbers of blocks are
found for comparisons involving a fish genome (circled in
black on Fig. 2). Such large numbers are in good accordance
with the large phylogenetic distance that separates fish
from tetrapodes. However, Actinopterygii species have
undergone a lineage specific WGD event that was
subsequently followed by a massive loss of gene duplicates. Some synteny blocks could result from these local
deletion events rather than from large chromosomal
rearrangements per se (see below). It is also possible that
these large numbers could partly result from an increase of
rearrangement rates after the WGD event. In yeasts, the
number of synteny blocks is more restrained, varying from
26 between Candida albicans and C. dubliniensis up to 744
between Debaryomyces hansenii and Pichia pastoris. The
number of blocks also exponentially increases along with
protein divergence but only between 8 and 36% of
divergence. At increasing phylogenetic distances, the
number of synteny blocks decreases (Fig. 2a). This trend
is most likely due to the repeated accumulation of
[(Fig._2)TD$IG]
G. Drillon, G. Fischer / C. R. Biologies 334 (2011) 629–638
633
Fig. 2. Comparative analysis of genome reorganization in 13 vertebrate and 18 yeast species (Table 1). Pairs of genes were considered as orthologs if their
products were reciprocal best-hits with at least 40% similarity in sequence and their sequences were less than 30% different in length as previously
described [39]. Synteny blocks were defined as series of neighboring pairs of orthologs separated by less than 5 nonneighboring reciprocal best-hits in the
two compared genomes. Synteny blocks were constructed for the 78 and 153 possible pairwise comparisons between the 13 vertebrate (orange diamonds)
and 18 yeast (purple diamonds) species, respectively. Black circles indicate pairwise comparisons involving at least one species that undergone a lineagespecific ancestral whole genome duplication (WGD) event (D. rerio, O. latipes and T. nigroviridis in vertebrates and S. cerevisiae and C. glabrata in yeasts).
Protein divergence values correspond to the mean divergence between syntenic reciprocal best hits for each pair of compared genomes. a. Evolution of the
number of synteny blocks as a function of protein divergence in vertebrates and yeasts. b. Evolution of the number of genes per block with increasing
phylogenetic distances. c. The number of synteny blocks is normalized by the mean size of the 2 compared genomes and plotted as log-scale. d. The number
of synteny blocks is used to approximate the number of rearrangements (comprising more than 5 genes) accumulated between 2 genomes for all
comparisons involving a level of protein divergence lower than 36%. For higher level of divergence, the number of synteny blocks cannot be used to
approximate the number of rearrangements because it decreases with increasing evolutionary distances (see a.). Rearrangement rates correspond to the
number of rearrangements divided by mean ortholog divergence between the compared paired of species. All 78 possible pairwise comparisons were taken
into account for vertebrates while only 55 out of the 153 pairwise comparisons were considered in yeast (below the threshold of 36% divergence).
breakpoints that lead to the reduction of the size of the
synteny blocks below the minimal threshold of 2
neighboring genes (Fig. 2b) and also to a less efficient
recognition of orthologous protein when divergence
increases (not shown). Two yeast genomes (S. cerevisiae
and Candida glabrata) have also undergone a WGD event
followed by rediploidization (circled in black in Fig. 2). But,
as opposed to vertebrates, all the comparisons that involve
either of these 2 species are scattered throughout the plot
because of their intermediate phylogenetic position
relative to other yeast species.
For comparable evolutionary distances, where ranges of
protein divergence overlap between yeast and vertebrate
(i.e. between 8 and 30% of protein divergence), the number
of synteny blocks between 2 vertebrate genomes is about 6
to 8-fold higher than between 2 yeast genomes (Fig. 2a).
This shows that despite a lower evolutionary range, the
raw level of chromosome map reorganization is much
higher in vertebrate than in yeast. This result shows that,
for comparable evolutionary distances, more chromosomal rearrangements occurred on average between 2 vertebrate genomes than between 2 yeast genomes. However,
the genome sizes being on average 200 times larger in
vertebrates, the physical density of synteny breakpoints
along chromosomes (measured by the number of synteny
blocks per Mb) is consistently higher in yeasts (between 5
and 65 blocks per Mb) than in vertebrates (between 0.01
and 2 blocks per Mb, Fig. 2c).
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G. Drillon, G. Fischer / C. R. Biologies 334 (2011) 629–638
For both yeast and vertebrate, the average number of
shared orthologs per synteny block decreases exponentially with increasing evolutionary distance until it
asymptotically reaches the threshold of 2 genes below
which it is impossible to recognize conserved synteny
blocks (Fig. 2b). Surprisingly, in the overlapping evolutionary range (i.e. between 8 and 30% of divergence), the
number of genes per block is higher in yeasts than in
vertebrates (54 vs 21 on average, respectively). This higher
number of genes per synteny block is best explained by the
conjunction of a higher gene density in yeast (only 4 times
as many genes in vertebrates than in yeasts while genome
sizes are on average 200 times larger) and a higher number
of rearrangements in vertebrates that is limited to only 6 to
8 times that of the yeast genomes.
Then, we estimated the rates of rearrangements by
approximating the number of synteny blocks to the
number of chromosomal rearrangements that occurred
since two species diverged from their last common
ancestor. Our analysis only accounts for rearrangements
involving more than 5 orthologous genes because we
tolerate up to 5 consecutive nonsyntenic homologs within
a synteny block. For instance, small inversions involving
less than 5 genes are not counted here. In yeast,
approximating the number of rearrangements to the
number of synteny blocks holds true only for pairwise
comparisons involving average protein divergence below
36%. For higher levels of divergence, the superimposition of
numerous rearrangements leads to the progressive destruction of recognizable synteny blocks and therefore to a
strong underestimation of the number of rearrangements
that actually occurred (see Fig. 2a and legend of Fig. 2d).
The rates of rearrangements correspond to the number of
rearrangements that occurred per unit of evolutionary
time, which corresponds here to 1% of divergence between
orthologous proteins (Fig. 2d). Mean rates of rearrangements are statistically different between the two groups
(40 4 vs 13 1 rearrangements/%divergence in vertebrates
and yeasts, respectively; T-test P-val = 5.4 10 23). On
average, rearrangement rates are 3-fold higher in vertebrates
than in yeasts.
In yeast, rearrangement rates do not convincingly
correlate with genome sizes (R2 = 0.11, P-val = 0.02) while
in vertebrate, rearrangement rates appear to be anticorrelated with genome sizes (R2 = 0.60, P-val = 5.8 10 9,
Fig. 2d) because small genomes seem to be more
rearranged. However, this anti-correlation uniquely relies
on the presence of the small duplicated fish genomes (all 3
fish used in the analysis have the smallest vertebrate
genomes) and vanishes when the corresponding data
points (circled in black in Fig. 2d) are removed from the
analysis (R2 = 0.23; p-value = 0.12). In fish genomes,
rearrangement rates are confounded by the lineage
specific rediploidisations subsequent to the WGD, which
only involve local deletions, not gene-reordering rearrangements. In reality, these fish genomes are remarkably
stable and show little rearrangements. For example,
Medaka (Oryzias latipes) has been subjected to zero
interchromosomal event since it splits from the pufferfish
(Tetraodon nigroviridis) lineage more than 100 Myrago
(Hugues Roest Crollius, pers. com.). Therefore approxi-
mating the number of rearrangements by the number of
synteny blocks for these postduplicated genomes might
lead to an overestimation of the rearrangement rates
in vertebrates. When comparisons involving duplicated
fish (O. latipes, D. rerio and T. nigroviridis) and yeast
(S. cerevisiae and C. glabrata) genomes are excluded from
the analysis, the mean rearrangement rate remains
significantly 2-fold higher in vertebrates than in yeasts
(27 2 vs 13 1 rearrangements/%divergence, respectively). It has been shown that both in yeasts and in vertebrates,
rearrangement rates are variable between individual
lineages [37–40]. For instance, rearrangement rates are
smaller between S. cerevisiae and Lachancea waltii (12.7)
than between S. cerevisiae and C. glabrata (15.9) and also
smaller between human and dog (20.9) than between
human and mouse (26.5), as previously reported [40,41].
Despite these lineage-specific variations, we show here
that the global rates of rearrangements are higher in
vertebrates than in yeasts, arguing against the hypothesis
of a molecular clock for rearrangements. However, because
of very large genome sizes in vertebrates, the average
rearrangement rate per Mb is about 50-fold higher in
yeasts than in vertebrates (1.04 vs 0.02 rearrangements/
%divergence/Mb in yeasts and vertebrates, respectively).
Because vertebrates have emerged within the Chordata
phylum approximately 450 Myr ago [42], the average rate
of 40 4 rearrangements/%divergence can be translated into
time unit and would correspond to a rate of 2 rearrangements/Myr (918 blocks on average divided by 450), close to
previous estimates on mammalian genome evolution (3.2
chromosomal rearrangements per million years on the
mouse branch from the murid rodent ancestor; 3.5 chromosomal rearrangements per million years on the rat branch;
and 1.6 chromosomal rearrangements per million years on
the human branch [37]). A similar translation would be less
reliable in yeast because estimated emergence time for the
Saccharomycotina subphylum vary between 400 and
1000 Myr ago [43] and also because at large evolutionary
distance (ortholog divergence greater than 36%) the number
of synteny blocks cannot be used to approximate the number
of rearrangements that actually happened.
Disclosure of interest
The authors declare that they have no conflicts of
interest concerning this article.
Acknowledgements
We thank Hugues Roest Crollius for critical reading of
the manuscript and for our regular scientific discussions
that have contributed to the realization of this work. We
are highly grateful to Jean-Luc Souciet, Bernard Dujon and
Claude Gaillardin for having given rise to the Genolevures
adventure and for allowing us to contribute.
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